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A Nuclear Gene of Eubacterial Origin in Euglena Gracilis Reflects Cryptic

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A Nuclear Gene of Eubacterial Origin in Euglena Gracilis Reflects Cryptic Proc. Natl. Acad. Sci. USA Vol. 92, pp. 9122-9126, September 1995 Evolution A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution (endosymbiotic gene transfer/eukaryotic evolution/introns/glyceraldehyde-3-phosphate dehydrogenase/kinetoplastids) KATRIN HENZE*,ABDELFATTAH BADRt MICHAEL WETIrERNt, RUDIGER CERFF*, AND WILLIAM MARTIN*§ *Institut fuir Genetik, Technische Universitat Braunschweig, Spielmannstrasse 7, D-38023 Braunschweig, Federal Republic of Germany; tInstitut fur Botanik, Technische Universitat Braunschweig, Mendelssohnstrasse 1, D-38023 Braunschweig, Federal Republic of Germany; and tBotany Department, Faculty of Science, Tanta University, Tanta, Egypt Communicated by Russell F. Doolittle, University of California, San Diego, CA, June 26, 1995 (received for review April 5, 1995) ABSTRACT Genes for glycolytic and Calvin-cycle glycer- may have entailed reduction and fusion of different genetic aldehyde-3-phosphate dehydrogenase (GAPDH) of higher eu- apparatuses which now comprise the three-membrane- karyotes derive from ancient gene duplications which oc- bounded chloroplast genome. (iii) Cytological (13, 14) and curred in eubacterial genomes; both were transferred to the DNA sequence (15) data indicate that the host cell ofEuglena's nucleus during the course of endosymbiosis. We have cloned secondary symbiosis shared a common ancestor with kineto- cDNAs encoding chloroplast and cytosolic GAPDH from the plastids, a group of nonphotosynthetic protists encompassing early-branching photosynthetic protist Euglena gracilis and trypanosomes and their relatives (16). Thus, in Euglena, nu- have determined the structure of its nuclear gene for cytosolic clear genes of endosymbiotic origin may have been transferred GAPDH. The gene contains four introns which possess un- twice: once to the algal nucleus and once more to the kineto- usual secondary structures, do not obey the GT-AG rule, and plastid nucleus. are flanked by 2- to 3-bp direct repeats. A gene phylogeny for Biochemical studies had indicated that Euglena, like other these sequences in the context of eubacterial homologues photosynthetic eukaryotes, possesses two distinct glyceralde- indicates that euglenozoa, like higher eukaryotes, have ob- hyde-3-phosphate dehydrogenase (GAPDH) enzymes, the tained their GAPDH genes from eubacteria via endosymbiotic Calvin-cycle GAPDH of chloroplasts (GapA, EC 1.2.1.13), (organelle-to-nucleus) gene transfer. The data further suggest and the glycolytic GAPDH of cytosol (GapC, EC 1.2.1.12) that the early-branching protists Giardia lamblia and Entamoe- (17); neither is encoded in Euglena's chloroplast DNA (cp- ba histolytica-which lack mitochondria-and portions of the DNA) (18). Here we show that the nuclear GapC and GapA trypanosome lineage have acquired GAPDH genes from eu- genes of Euglena, as in other eukaryotes, are descendants of bacterial donors which did not ultimately give rise to con- ancient gene duplications which occurred in eubacterial ge- temporary membrane-bound organelles. Evidence that "cryp- nomes (4, 19). We argue that during evolution, the kineto- tic" (possibly ephemeral) endosymbioses during evolution plastid lineage as well as the amitochondriate protists Giardia may have entailed successful gene transfer is preserved in and Entamoeba have independently obtained GAPDH genes protist nuclear gene sequences. from eubacteria through cryptic endosymbiosis-i.e., in an endosymbiotic context resulting in abortive organelle genesis. Some genes for proteins essential to chloroplasts and mito- We also report the structure of Euglena's expressed nuclear chondria were encoded in the genomes of free-living anteced- GapC gene.l ents of these organelles and were transferred to the nucleus during evolution. This process, endosymbiotic gene transfer, is MATERIALS AND METHODS a special case of interkingdom horizontal gene transfer and took place in a biologically meaningful context. The contem- Isolation of Recombinant Clones. Euglena cultures (SAG porary protein products of these genes are synthesized on 1224-5/25) were grown as described (20) under a 14-hr cytosolic ribosomes and reimported into the organelle of their light/10-hr dark regime aerated with 1.5% CO2. Nucleic acid genetic origin. Although intracellular gene transfer is an isolation and cDNA cloning were performed as described (21). ongoing process, the evidence suggests that most genes were The cDNA library was screened by plaque hybridization (4) transferred during the early phases of endosymbiosis (1-4). It with an end-labeled oligonucleotide, 5'-TGGTAYGAYAAN- is conceivable that DNA transferred from organelles to the GART-3'. About 106 recombinants of an Mbo I genomic nucleus may have carried not only coding sequences, but also library in AEMBL4 (22) were screened by plaque hybridization the forerunners of spliceosomal introns now widespread in with the random-labeled Not I insert of pEGC20 (encoding eukaryotic nuclei (5-7). Little is known about nuclear genes GapC; see Results). Five clones containing a 4.2-kb HindlIl from protists which branched early in eukaryotic evolution. fragment identified by Southern hybridization of genomic Euglena gracilis is well suited for the study of endosymbiosis DNA (data not shown) were purified. The hybridizing Hindlll and organellar gene transfer. (i) Euglena's plastids are sur- fragment of AEGCgllO was subcloned into pBluescript vectors rounded by three membranes instead of two and possess (Stratagene) and sequenced. Other molecular methods were as chlorophylls a and b, findings which led to the suggestion (8) described (22). that Euglena's plastids may have arisen through engulfment of Phylogenetic Analysis. The amino acid alignment (available a eukaryotic alga (secondary endosymbiosis), a notion sup- upon request) from which nucleotide sequences (368 codons ported by molecular sequence analyses (9, 10). (ii) Whereas per sequence) were aligned was produced with the LINEUP some algae of secondary symbiotic origin possess a vestigial program of the WISGEN package (23). A matrix of divergence nucleus (nucleomorph) of the eukaryotic symbiont (11, 12), Euglena does not. Evolutionary degeneration of the symbiont Abbreviations: GAPDH, glyceraldehyde-3-phosphate dehydrogenase; cpDNA, chloroplast DNA. §To whom reprint requests should be addressed. The publication costs of this article were defrayed in part by page charge IThe sequences from Euglena gracilis reported in this paper have been payment. This article must therefore be hereby marked "advertisement" in 4jeposited in the GenBank data base [accession nos. L21903 (GapC accordance with 18 U.S.C. §1734 solely to indicate this fact. cDNA), L21904 (GapA cDNA), and L39772 (GapC gene)]. 9122 Evolution: Henze et al. Proc. Natl. Acad. Sci. USA 92 (1995) 9123 at nonsynonymous sites (24) was used to construct a neighbor- teria have not been reported, but sufficient isolated eubacterial joining tree (25). The topology was tested by bootstrap neigh- gap gene sequences exist in the data base to reveal that the bor-joining analysis using the Dayhoff matrix (PHYLIP 3.5) common eubacterial ancestor had four or more gap genes. between protein sequences. Members of the ancestral gene family may have been lost independently in different eubacterial lineages or have not RESULTS AND DISCUSSION been characterized to date, as indicated by open branches in tI-tIV. Comparisons of sequences across different subtrees GAPDH: A Eubacterial Gene Family. Previous work indi- reveal an average of about 50% amino acid identity. Within cated that genes for eukaryotic GAPDH enzymes are descen- subtrees, average amino acid identity is about 60% or greater, dants of an ancient gene family which existed in the common except within subtree tlIl (45-50%), which contains the rapidly ancestor of extant eubacteria (4, 19, 26). This view is supported evolving Anabaena gap3 and E. coli gap2 sequences and by the GAPDH gene phylogeny in Fig. 1. To date, GAPDH receives only very weak support from bootstrap analysis, gene families of at least three members have been character- making the identification of this subtree tentative. ized in two eubacteria, Anabaena variabilis (4) and E. coli (28, Subtree tI contains by far the greatest number of sequenced 29) (the third E. coli sequence is not complete; GenBank eubacterial genes. E. coli gapl and the Serratia sequence were accession no. L09067). For gapl, gap2, and gap3 of E. coli, chosen to represent the roughly 60 sequences reported from orthologous genes have been characterized in other free-living enterics (ref. 30 and GenBank release 84). The partial se- eubacteria, as shown in the schematic topologies (subtrees) tI, quence of a gapl gene from the ,-purple bacterium Pseudo- tIl, and tIV in Fig. 1. For Anabaena gap2, orthologues have monas solanacearum was recently reported (GenBank acces- been characterized only in cyanobacteria (unpublished data) sion no. L19269); phylogenetic analysis of the C-terminal 75 aa and in the nuclei of photosynthetic eukaryotes, to which they which have been sequenced for that gene suggests that it is were transferred from the antecedents of modern chloroplasts orthologous to E. coli and Anabaena gapl, branching robustly (tII). Broad-scale surveys of GAPDH gene diversity in eubac- within tI (data not shown), supporting this interpretation of Species and gene Taxon Enzymeor genecompartmentcluster Introntype Schematic Eubacterial Topology Zea GapC Chlorophyta cytosol GT-AG Chondnus
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